Toxicity of Monoterpene Structure, Diversity and Concentration to Mountain Pine Beetles, Dendroctonus ponderosae: Beetle Traits Matter More
A high diversity of plant defenses may be a response to herbivore diversity or may be collectively more toxic than single compounds, either of which may be important for understanding insect-plant associations. Monoterpenes in conifers are particularly diverse. We tested the fumigant toxicity of four monoterpenes, alone and in combination, to mountain pine beetles, Dendroctonus ponderosae, in the context of the beetles' individual body traits. Chemical structures of tested monoterpene hydrocarbons had modest effects on beetle survival, mass loss, water content and fat content, with (R)-(+)-limonene tending to be more toxic than (−)-α-pinene, (−)-β-pinene, and (+)-3-carene. Monoterpene diversity (all qualitative combinations of one to four monoterpenes) did not affect toxicity. Concentration (0 to 1200 ppm) of individual monoterpenes was a strong determinant of toxicity. Beetle body size and body condition index strongly and positively affected survival during monoterpene treatments. Larger beetles in better condition lost proportionally less mass during exposure, where proportion mass loss negatively affected survivorship. Toxicity was much more associated with water loss than with fat loss, suggesting that a main cost of detoxification is excretion, a process that has received little attention. These results provide insight into the determinants of beetle success in historic and novel hosts that differ in monoterpene composition and concentration. We also suggest that water availability will affect beetle success directly through their ability to tolerate detoxification as well as indirectly through host responses to drought.
KeywordsPlant defences Monoterpenes Pinus Scolytinae Fumigant toxicity Body size
Funding for this study was provided by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to MLR. We thank H. Peralta-Vázquez, M. Fenton, T. Rajabi and J. Zawalykut for their assistance in the lab. K. Raffa, W. Francke and an anonymous reviewer provided helpful comments.
- Byers JA (1995) Host-tree chemistry affecting colonization in bark beetles. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects, 2nd edn. Chapman and Hall, New York, pp 156–213Google Scholar
- Cano-Ramirez C, Lopez MF, Cesar-Ayala AK, Pineda-Martinez V, Sullivan BT, Zuniga G (2013) Isolation and expression of cytochrome P450 genes in the antennae and gut of pine beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae) following exposure to host monoterpenes. Gene 520:47–63CrossRefPubMedGoogle Scholar
- Cook SP, Hain FP (1988) Toxicity of host monoterpenes to Dendroctonus frontalis and Ips calligraphus (Coleoptera: Scolytidae). J Entomol Sci 23:287–292Google Scholar
- Gershenzon J, Fontana A, Burow M, Wittstock U, Degenhardt J (2012) Mixtures of plant secondary metabolites: metabolic origins and ecological benefits. In: Iason GR, Dicke M, Hartley S (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 56–77CrossRefGoogle Scholar
- Geyer HJ, Scheunert I, Rapp K, Gebefugi I, Steinberg C, Kettrup A (1993) The relevance of fat content in toxicity of lipophilic chemicals to terrestrial animals with special reference to dieldrin and 2,3,7,8-tetrachlorodibeno-p-dioxin (TCDD). Ecotoxicol Environ Saf 26:45–60CrossRefPubMedGoogle Scholar
- Karise R, Mänd M (2015) Recent insights into sublethal effects of pesticides on insect respiratory physiology. Open Access Insect Physiology 31Google Scholar
- Robert JA, Pitt C, Bonnett TR, Yuen MM, Keeling CI, Bohlmann J, Huber DP (2013) Disentangling detoxification: gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLoS One 8:e77777CrossRefPubMedPubMedCentralGoogle Scholar
- Romeo JT, Saunders JA, Barbosa P (eds) (1996) Phytochemical diversity and redundancy in ecological interactions, vol 30. Recent Advances in Phytochemistry. Plenum Press, New YorkGoogle Scholar
- Safranyik L, Carroll AL (2006) The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In: Safranyik L, Wilson B (eds) The mountain pine beetle: a synthesis of its biology and Management in Lodgepole Pine. Natural Resources Canada, Canadian Forest ServiceGoogle Scholar
- SAS Institute Inc. (2015). JMP 12.0. Cary, North CarolinaGoogle Scholar